Wilson Bull., 97(2), 1985,
pp. 183-190
BREEDING ROBINS AND NEST PREDATORS: EFFECT
OF PREDATOR TYPE AND DEFENSE STRATEGY ON
INITIAL VOCALIZATION
PATTERNS
BRADLEY M. GOTTFRIED, KATHRYN ANDREWS, AND MICHAELA HAUG
Breeding birds are subject to intense nest-predation pressure by a variety
of predators (Gottfried 1978, Gottfried and Thompson 1978). To counteract this pressure, a number of antipredator adaptations have evolved
in birds. These adaptations appear to involve nest concealment, distraction displays, and colonial nesting (Skutch 1976). Another antipredator
strategy is active nest defense. By imposing the possibility of injury on a
predator, a breeding bird may be successful in protecting its nest. Indeed,
experimental studies have shown that nesting birds do attack models of
nest predators (see Gottfiied 1979 and references cited therein). As expected, the intensity of defense increases through the breeding cycle as
the amount of parental investment increases (Shields 1984). There is also
evidence that birds respond in a different manner to different types of
nest predators (Gottfried 1979).
Actual fighting between two animals can be costly in terms of risk of
physical injury as well as in time and energy. It has been hypothesized
that mechanisms have evolved to reduce the incidence of these interactions (Maynard Smith 1974). As most contests are asymmetric (e.g., the
contestants are not equally matched), it is important for each contestant
to assess the likelihood that it will win a contest. If, after assessing the
situation, a contestant finds that its chances of winning an encounter are
low, it may well forgo further interaction, and retreat (Parker 1974). Threat
displays may be an important cue in determining the formidability of a
particular opponent. Another potential source of information about an
opponent may be in its repertoire of vocalizations. Smith (1977) has
shown that auditory signals have evolved as an effective way of transmitting information among organisms. Alternative explanations have also
been offered (Dawkins and Krebs 1978).
Birds possess a unique repertoire of sounds that are used in territory
defense, courtship, and flock maintenance; and a number of studies have
shown that birds have the ability to use vocalizations to convey contextual
information about motivation levels. Vocalizations conceivably could be
used by a nest predator in assessing motivation levels and defense strategy
of a breeding bird, or they could be used to signal information about
predator-type and form of defense strategy to conspecifics and thus could
be used to coordinate nest defense. Predator-induced vocalizations have
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been studied extensively in ground squirrels. These organisms give predator-specific types of alarm calls that may also encode information about
the predator’s activity patterns (Owings and Virginia 1978, Leger et al.
1980, Owings and Leger 1980, Robinson 1980). There have been few
similar studies of birds, and most were not experimental (Morton and
Shalter 1977, Greig-Smith 1980).
This paper reports on a study in which we examined the vocalizations
of American Robins (Turdus migratorius) in relation to models of two
types of nest predators. We were particularly interested in determining
whether initial vocalizations accurately reflected later nest defense strategies (attack or not attack the model), and in the type of predator eliciting
the calls.
METHODS AND MATERIALS
The study was conductedfrom April through July in 1980 and 1981 in old-field habitats
in and around St. Paul, Minnesota. We attempted to locate nests soon after egglaying was
initiated. Each nest was tested three to five days after the start of incubation. The following
techniquewas used for each test. A stuffedBlue Jay (Cyanocitta cristatu)or a rubber snake
model was affixed to the nest after the female left to feed. After positioning the predator,
we retreatedto a concealedposition approximately 15 m away, from which we could observe
subsequentevents at the nest. Each test lasted about five min. We useda Uher 4000 Report
Moniter tape recorderand a Dan Gibson P650 microphone to record the vocalizations.The
tapeswere later analyzed with a Ray sonographmodel 606 1B. In all tests,the vocalizations
uttered by the female within five set of its return to the nest were analyzed. These vocalizations were referred to as the Initial Response Repertoire (IRR). The response of the
nesting bird to the predator model was also ranked using the scalepresentedin Table 1.
RESULTS
Robins primarily used two types of vocalizations in their responses to
predator models (Fig. 1): “chirps” and “chucks.” “Chirps” were more
complex than “chucks,” being longer in duration and composed of a wider
range of frequencies.
The type of predator model presented influenced the type of vocalization included in a bird’s IRR. Eighty-eight percent of the robins tested
with the stuffed Blue Jay included “chirps” in their IRR, but only 42%
uttered “chirps” in response to the snake (x2 = 8.62, df = 1, P < 0.05).
The proportion of robins that included “chucks” in their IRR to the jay
was not significantly different from those that included “chucks” to the
snake (x2 = 0.39, df = 1, P < 0.05).
“Chirps” were significantly more likely to be included in the IRR of
birds that ultimately attacked a model than those that did not attack (92%
vs 41%; x2 = 8.29, df = 1, P < 0.05). “Chucks,” on the other hand, were
more likely to be included in the IRR of robins that did not later attack
the predator models (73% vs 38%; x2 = 4.82, df = 1, P < 0.05).
Gottfried et al.
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ROBINS AND NEST PREDATORS
TABLE
185
1
SCALEUSEDTODETERMINETHEAGGRESSIONRESPONSEINDEXOFROBINS
Aggression
Movement
pattern
0 = No response
1 = Approach predator (< 5 approaches
and retreats/min) no attacks
0 = No movement
2 = Frequent approaches(> 5 approachesand retreats/min) no attacks)
3 = Few attacks (~5 strikes on predator/
min)
2 = Medium movement (15-30 changes
in position/min)
1 = Little movement (~5 changesin positiommin)
3 = Frenzied movement (>30 changesin
position/min)
4 = Frequent attacks(> 5 strikes on
predator/min)
Robins that ultimately attacked a jay model were more likely to utter
“chirps” than birds that did not attack the jay (x2 = 5.03, df = 1, P <
0.05; Table 2), while “chucks” were more likely to be given by birds that
did not later attack the jay models than by those birds that did (x2 = 3.7 1,
df = 1, P < 0.05). Too few robins attacked the snake model to permit a
statistical analysis of the data.
To explore the fine details of the “alarm” vocalizations, sonograph
tracings were made, and data were collected and subsequently analyzed
using 2 x 2 Analyses of Variance (ANOVA) in an effort to examine possible differences.
The two main effects in the ANOVA were predator type and ultimate
form of defense. Three of the seven vocal parameters studied were significantly related to the type of predator model presented (Table 3). Robins
uttered twice as many vocalizations/30 set (particularly “chirps”) in response to the jay model as they did to the snake. This was caused by
significant differences in the number of “chirps”/30 set; the number of
“chucks”/30 set was not affected. The increase in the number of vocalizations/30 set was at the expense of the duration of intervals between
notes and not in note length. The ANOVA suggests that the quantitative
changes in the IRR in relation to ultimate defense strategy somewhat
parallel that of predator type, with birds that later attacked the model
uttering significantly more notes in general, and “chirps” in particular,
than birds that did not ultimately attack the model.
Robins that ultimately attacked the jay model included a significantly
greater number of vocalizations/30 set in their IRR than those birds that
did not attack the model (Table 3). These pre-attack vocalizations con-
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lo-
A
?
Y
56
h
A
I
0.5
1.0
1.5
SECONDS
FIG. 1. Sample sonographtracing of a robin vocalization. Notes with an A are “chirps”,
those with a B are “chucks.”
tained significantly more “chirps” and fewer “chucks” than those robins
that did not attack the jay model. Robins that ultimately attacked the jay
model also uttered “chucks” whose frequency was significantly different
from those birds that did not attack the model.
The IRR of robins that ultimately attacked the snake model contained
significantly more notes/30 set and significantly more “chucks” than the
IRR of robins that did not attack the snake. The attacking robins also
gave shorter “chirp” vocalizations than robins that did not later attack.
The IRR of robins prior to attacks on the jay and snake models did
not contain significantly different numbers of vocalizations/30 sec. This
was due to significant but opposite trends in the number of “chirps” and
“chucks” (Table 3). Robins that later attacked the jay model uttered an
average of 60.3 “chirps”/30 set, compared to only 20.5/30 set in those
that later attacked the snake. On the other hand, the number of “chucks”/
30 set was 4 1.8 in the snake experiments and only 1.1 in the jay experiments. Attacks on the jay model were also preceded by “chirps” that
contained a shorter time interval between notes than those in the IRR
which preceded attacks on the snake model.
The data presented so far indicate that several vocal parameters, particularly the number of vocalizations/30 set, are related to defense strategy. As the intensity of the responses to the model varied, the data were
analyzed with a Spearman Rank Correlation Test to determine if any of
the seven vocal parameters was correlated with intensity of nest defense.
The intensity of defense was correlated positively with the total number
of vocalizations/30 set (rs = 0.76, P < 0.05), the number of “chirps”/30
set (rs = 0.75, P < 0.05), and low (rs = 0.57, P < 0.05) and high (rs =
0.58, P < 0.05) frequency of “chirps”. Duration of “chirps” (Y, = 0.33,
Gottfriedet al.
l
ROBINS
AND
TABLE
NUMBER OF AMERICAN
ROBINS UTTERING
187
NEST PREDATORS
2
“CHIRPS”
AND “CHUCKS”
IN RELATION TO
PREDATOR AND LIKELIHOOD OF ATTACK
Predator model
N
No.
giving“chirps” (%)
No. giving“chucks” (%)
Blue Jay
Attack
No attack
22
10
22 (100)
6 (60)
6 (27)
10 (100)
Total
32
28 (88)
16 (50)
Snake
4
2 (50)
No attack
20
8 (40)
6 (30)
Total
24
10 (42)
10 (42)
Attack
4 (100)
P > 0.05) or their spacing (Y, = 0.45, P > 0.05) were not correlated with
the levels of aggression.
DISCUSSION
Our results suggest that certain parameters, specifically the number of
vocalizations a robin utters, the number of major vocalization types
(“chirps”), and certain frequency parameters are related to predator type,
future defense decisions, and the intensity of future nest defense.
These results are consistent with earlier studies of monkeys and ground
squirrels. Vervet Monkeys (Cercopithecusaethiops) possess large repertoires of predator-specific alarm calls (Struhsaker 1967, Cheney and Seyfarth 198 1). Broadcast of these signals caused free-ranging monkeys to
take appropriate defensive measures (Seyfarth et al. 1980). The vocal
signals of ground squirrels, although lower in diversity, also show evidence
of being predator-specific (Owings and Virginia 1978, Robinson 1980).
For example, California Ground Squirrels (Spermophilusbeecheyz]emit
“chatters” and “chats” in the presence of terrestrial predators, and “whistles” when raptors are present. Detailed spectrographic examination of
vocalizations was conducted by Owings and Leger (1980) and Leger et
al. (1980). “Chatters” evoked by raptors and terrestrial predators were
distinct from each other. Owings and Leger (1980) also found the rate of
calling to be related to the type of predator. Ground squirrels communicate
predator identity through the use of predator-specific vocalization, graded
signals, and rates of calling. These data agree with those we collected on
robins. Robins were more likely to emit “chirps” than “chucks” in response to the jay model, but were equally likely to utter “chirps” and
Gottfried et al.
l
ROBINS AND NEST PREDATORS
189
“chucks” to the snake. Our study suggeststhat the ultimate defense strategy (attack or not attack) and intensity of future defense may be encoded
in a robin’s predator-induced vocalizations. In addition to the quantitative
data presented, this idea is supported by qualitative observations at robin
nests. In most of the tests where the robins ultimately attacked the predator
models, their vocalizations attracted other robins as well as Common
Grackles (Quiscalusquiscula)and Field Sparrows (Spizella pusilla) to the
area around the nest. Breeding robins tended to attack these new arrivals,
but were usually unable to drive them away. We conducted similar predator-induced vocalization studies with Gray Catbirds (Dumetella carolinensis). During these tests, other catbirds were attracted by the vocalizations of the nesting catbird being tested, but unlike robins, these arrivals
were tolerated and they may have been involved in attacking the predator
models. Robins and catbirds that did not ultimately attack the predator
model did not attract other birds to the general area around their nests.
By uttering certain numbers and types of vocalizations a bird might be
able to gain assistance from other birds in the area in its defense against
the predator. Even in our observations of robins where other birds were
not involved in defense, the presence of additional agitated birds may be
enough to dissuade a predator from continuing its attempt to prey on the
contents of the nest.
SUMMARY
The study was conducted to determine if predator-induced vocalizations of breeding
American Robins (Turdus migrutorius) were related to predator identity (Blue Jay [Cyanocittu cristata] or snake),laterdefensestrategy
(attackor not attackmodel),andintensity
of future defense. Robins used two types of vocalizations in their response to the nest
predators:“chirps” and “chucks.”
Nesting robins were significantlymore likely to utter “chirps” than “chucks” in testswith
a stuffedBlue Jay. All birds that later attackedthe jay included “chirps” in their repertoire;
all those that did not attack included “chucks” in their repertoire. In experiments with a
snake model, both types of vocalizations were equally likely to be given. The number of
vocalizations/30 set and the number of “chirps”/30 set were consistentlyrelated to predator
type, future defense strategy,and intensity of future defense.
ACKNOWLEDGMENTS
We wish to thank R. Christman and C. and D. Fiedler for their assistanceand encouragement. Two referees, D. Shedd and W. M. Shields provided valuable suggestions.F.
Vukmonich provided vital electronicsassistance.The studywas funded by National Science
Foundation Grant CDP-8010620, and by a National Science Foundation Undergraduate
ResearchParticipation Grant.
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DEPT. BIOLOGY,
COLL. ST. CATHERINE,
ADDRESS BMG: DEPT. BIOLOGY,
GEORGIA
31419.)
ACCEPTED
ST. PAUL, MINNESOTA
ARMSTRONG
5 JAN. 1985.
5 5 105. (PRESENT
STATE COLLEGE,
SAVANNAH,